{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,30]],"date-time":"2026-09-30T07:52:11Z","timestamp":1790754731198,"version":"4.1.0"},"reference-count":22,"publisher":"Journal of Neurosurgery Publishing Group (JNSPG)","issue":"1","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2024,7,1]]},"abstract":"<jats:sec>\n<jats:title>OBJECTIVE<\/jats:title>\n<jats:p>Indirect revascularization is a common and effective treatment for pediatric moyamoya disease. However, in several cases postoperative angiogenesis is not sufficient. It is not fully understood which factors are involved in the development of postoperative collateral circulation. In this study, the authors aimed to elucidate the factors related to postoperative angiogenesis in indirect revascularization.<\/jats:p>\n<\/jats:sec>\n<jats:sec>\n<jats:title>METHODS<\/jats:title>\n<jats:p>Among the patients who underwent indirect revascularization for moyamoya disease from January 2015 to December 2022, those whose angiogenesis was evaluated using angiography were included. Age, onset symptoms, comorbidities, preoperative imaging findings, surgical details, perioperative complications, postoperative imaging findings, and modified Rankin Scale (mRS) score at the last outpatient visit were retrospectively examined.<\/jats:p>\n<\/jats:sec>\n<jats:sec>\n<jats:title>RESULTS<\/jats:title>\n<jats:p>Ninety cases (53 patients; 37 bilateral, 16 unilateral) were included. Sixty-eight cases (75.6%) were symptomatic. The mean age at surgery was 7.9 years, and the mean postoperative follow-up duration was 48.5 months. Frontotemporal encephalo-duro-arterio-synangiosis (EDAS) was performed in all cases, and simultaneous frontal encephalo-galeo-synangiosis (EGS) was performed in 34 cases. Postoperative angiography revealed insufficient angiogenesis in 14 of 90 cases (15.6%) after frontotemporal EDAS and in 8 of 34 cases (23.5%) after frontal EGS. A high degree of ivy sign depicted on preoperative MRI was found to be significantly correlated with good angiogenesis after both surgical procedures (p = 0.00030 for EDAS and p = 0.0039 for frontal EGS). In addition, an advanced preoperative Suzuki stage was significantly correlated with good postoperative angiogenesis after EDAS (p = 0.00040). Good angiogenesis was significantly correlated with postoperative improvement of the ivy sign in both procedures (p = 0.0005 in EDAS and p = 0.030 in frontal EGS) as well as correlated with a better mRS score at long-term follow-up after EDAS (p = 0.018).<\/jats:p>\n<\/jats:sec>\n<jats:sec>\n<jats:title>CONCLUSIONS<\/jats:title>\n<jats:p>Preoperative ivy sign and Suzuki classification are related to the degree of angiogenesis achieved after indirect revascularization for pediatric moyamoya disease.<\/jats:p>\n<\/jats:sec>","DOI":"10.3171\/2024.2.peds23414","type":"journal-article","created":{"date-parts":[[2024,4,13]],"date-time":"2024-04-13T02:25:55Z","timestamp":1712975155000},"page":"111-117","source":"Crossref","is-referenced-by-count":8,"title":["Indirect revascularization for pediatric moyamoya disease"],"prefix":"10.3171","volume":"34","author":[{"given":"Shotaro","family":"Ogawa","sequence":"first","affiliation":[{"name":"Department of Neurosurgery, National Center for Child Health and Development, Tokyo, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hideki","family":"Ogiwara","sequence":"additional","affiliation":[{"name":"Department of Neurosurgery, National Center for Child Health and Development, Tokyo, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1754","reference":[{"issue":"1","key":"b1","series-title":"Neurosurgery","first-page":"93","article-title":"Moyamoya disorder in the United States","volume":"71","author":"Starke RM","year":"2012","unstructured":"Starke RM, Crowley RW, Maltenfort M,  Moyamoya disorder in the United States. Neurosurgery. 2012;71(1):93\u201399."},{"issue":"2","key":"b2","series-title":"Stroke","first-page":"476","article-title":"Surgical management of moyamoya disease","volume":"49","author":"Acker G","year":"2018","unstructured":"Acker G, Fekonja L, Vajkoczy P. Surgical management of moyamoya disease. Stroke. 2018;49(2):476\u2013482."},{"issue":"1","key":"b3","series-title":"J Stroke","first-page":"21","article-title":"Moyamoya disease: treatment and outcomes","volume":"18","author":"Kim T","year":"2016","unstructured":"Kim T, Oh CW, Bang JS, Kim JE, Cho WS. Moyamoya disease: treatment and outcomes. J Stroke. 2016;18(1):21\u201330."},{"issue":"4","key":"b4","series-title":"Cerebrovasc Dis","first-page":"361","article-title":"Characterization of direct and indirect cerebral revascularization for the treatment of European patients with moyamoya disease","volume":"32","author":"Czabanka M","year":"2011","unstructured":"Czabanka M, Pe\u00f1a-Tapia P, Scharf J,  Characterization of direct and indirect cerebral revascularization for the treatment of European patients with moyamoya disease. Cerebrovasc Dis. 2011;32(4):361\u2013369."},{"issue":"3","key":"b5","series-title":"Acta Neurochir (Wien)","first-page":"269","article-title":"Neovascularization (angiogenesis) after revascularization in moyamoya disease. Which technique is most useful for moyamoya disease?","volume":"142","author":"Houkin K","year":"2000","unstructured":"Houkin K, Kuroda S, Ishikawa T, Abe H. Neovascularization (angiogenesis) after revascularization in moyamoya disease. Which technique is most useful for moyamoya disease?. Acta Neurochir (Wien). 2000;142(3):269\u2013276."},{"issue":"7","key":"b6","series-title":"Childs Nerv Syst","first-page":"2233","article-title":"The feasibility of performing multiple burr hole surgery in pediatric moyamoya patients as a response to failed mEDAS","volume":"37","author":"Hwang JK","year":"2021","unstructured":"Hwang JK, Park EK, Kim J, Kang HC, Kim DS, Shim KW. The feasibility of performing multiple burr hole surgery in pediatric moyamoya patients as a response to failed mEDAS. Childs Nerv Syst. 2021;37(7):2233\u20132238."},{"issue":"5","key":"b7","series-title":"J Neurosurg","first-page":"1520","article-title":"Editorial. Direct versus indirect bypass for moyamoya disease: ongoing controversy","volume":"126","author":"Teo MK","year":"2017","unstructured":"Teo MK, Madhugiri VS, Steinberg GK. Editorial. Direct versus indirect bypass for moyamoya disease: ongoing controversy. J Neurosurg. 2017;126(5):1520\u20131522."},{"key":"b8","series-title":"World Neurosurg","first-page":"179","article-title":"Perioperative complications and long-term outcomes after bypasses in adults with moyamoya disease: a systematic review and meta-analysis","volume":"92","author":"Sun H","year":"2016","unstructured":"Sun H, Wilson C, Ozpinar A,  Perioperative complications and long-term outcomes after bypasses in adults with moyamoya disease: a systematic review and meta-analysis. World Neurosurg. 2016;92:179\u2013188."},{"issue":"1","key":"b9","series-title":"Clin Neuroradiol","first-page":"91","article-title":"Time course of neoangiogenesis after indirect bypass surgery for moyamoya disease. Comparison of short-term and long-term follow-up angiography","volume":"30","author":"Zhao Y","year":"2020","unstructured":"Zhao Y, Lu J, Zhang Q,  Time course of neoangiogenesis after indirect bypass surgery for moyamoya disease. Comparison of short-term and long-term follow-up angiography. Clin Neuroradiol. 2020;30(1):91\u201399."},{"issue":"11","key":"b10","series-title":"Eur Radiol","first-page":"8364","article-title":"Encephaloduroarteriosynangiosis (EDAS) treatment of moyamoya syndrome: evaluation by computed tomography perfusion imaging","volume":"31","author":"Guo X","year":"2021","unstructured":"Guo X, Yuan X, Gao L,  Encephaloduroarteriosynangiosis (EDAS) treatment of moyamoya syndrome: evaluation by computed tomography perfusion imaging. Eur Radiol. 2021;31(11):8364\u20138373."},{"issue":"1","key":"b11","series-title":"J Neurosurg","first-page":"98","article-title":"Predictors of neoangiogenesis after indirect revascularization in moyamoya disease: a multicenter retrospective study","volume":"132","author":"Zhao Y","year":"2019","unstructured":"Zhao Y, Li J, Lu J,  Predictors of neoangiogenesis after indirect revascularization in moyamoya disease: a multicenter retrospective study. J Neurosurg. 2019;132(1):98\u2013108."},{"issue":"4","key":"b12","series-title":"J Neurosurg Pediatr","first-page":"458","article-title":"Ivy sign: a diagnostic and prognostic biomarker for pediatric moyamoya","volume":"29","author":"Montaser AS","year":"2021","unstructured":"Montaser AS, Lalgudi Srinivasan H, Staffa SJ,  Ivy sign: a diagnostic and prognostic biomarker for pediatric moyamoya. J Neurosurg Pediatr. 2021;29(4):458\u2013466."},{"issue":"1","key":"b13","series-title":"Cerebrovasc Dis","first-page":"19","article-title":"The leptomeningeal ivy sign on fluid-attenuated inversion recovery images in moyamoya disease: positron emission tomography study","volume":"36","author":"Kaku Y","year":"2013","unstructured":"Kaku Y, Iihara K, Nakajima N,  The leptomeningeal ivy sign on fluid-attenuated inversion recovery images in moyamoya disease: positron emission tomography study. Cerebrovasc Dis. 2013;36(1):19\u201325."},{"issue":"3","key":"b14","series-title":"Neurosurgery","first-page":"401","article-title":"Surgical treatment of moyamoya disease in pediatric patients\u2014comparison between the results of indirect and direct revascularization procedures","volume":"31","author":"Matsushima T","year":"1992","unstructured":"Matsushima T, Inoue T, Suzuki SO, Fujii K, Fukui M, Hasuo K. Surgical treatment of moyamoya disease in pediatric patients\u2014comparison between the results of indirect and direct revascularization procedures. Neurosurgery. 1992;31(3):401\u2013405."},{"key":"b15","series-title":"Ther Adv Chronic Dis","first-page":"2040622320960004","article-title":"What and why: the current situation and future prospects of \"ivy sign\" in moyamoya disease","volume":"11","author":"Yu J","year":"2020","unstructured":"Yu J, Du Q, Xie H, Chen J, Chen J. What and why: the current situation and future prospects of \"ivy sign\" in moyamoya disease. Ther Adv Chronic Dis. 2020;11:2040622320960004."},{"issue":"5-6","key":"b16","series-title":"Cerebrovasc Dis","first-page":"223","article-title":"Ivy sign predicts ischemic stroke recurrence in adult Moyamoya patients without revascularization surgery","volume":"47","author":"Nam KW","year":"2019","unstructured":"Nam KW, Cho WS, Kwon HM,  Ivy sign predicts ischemic stroke recurrence in adult Moyamoya patients without revascularization surgery. Cerebrovasc Dis. 2019;47(5-6):223\u2013230."},{"key":"b17","series-title":"Front Neurol","first-page":"661952","article-title":"Non-invasive urinary biomarkers in moyamoya disease","volume":"12","author":"Sesen J","year":"2021","unstructured":"Sesen J, Driscoll J, Moses-Gardner A, Orbach DB, Zurakowski D, Smith ER. Non-invasive urinary biomarkers in moyamoya disease. Front Neurol. 2021;12:661952."},{"issue":"3","key":"b18","series-title":"Neurosurg Rev","first-page":"2305","article-title":"Impact of RNF213 founder polymorphism (p.R4810K) on the postoperative development of indirect pial synangiosis after direct\/indirect combined revascularization surgery for adult Moyamoya disease","volume":"45","author":"Ito M","year":"2022","unstructured":"Ito M, Kawabori M, Sugiyama T,  Impact of RNF213 founder polymorphism (p.R4810K) on the postoperative development of indirect pial synangiosis after direct\/indirect combined revascularization surgery for adult Moyamoya disease. Neurosurg Rev. 2022;45(3):2305\u20132313."},{"issue":"2","key":"b19","series-title":"Cerebrovasc Dis","first-page":"171","article-title":"Impact of RNF213 c.14576G>A variant on the development of direct and indirect revascularization in pediatric moyamoya disease","volume":"52","author":"Kawabori M","year":"2023","unstructured":"Kawabori M, Ito M, Kazumata K,  Impact of RNF213 c.14576G>A variant on the development of direct and indirect revascularization in pediatric moyamoya disease. Cerebrovasc Dis. 2023;52(2):171\u2013176."},{"issue":"8","key":"b20","series-title":"AJNR Am J Neuroradiol","first-page":"1574","article-title":"Elevated cerebral blood volume contributes to increased FLAIR signal in the cerebral sulci of propofol-sedated children","volume":"35","author":"Harreld JH","year":"2014","unstructured":"Harreld JH, Sabin ND, Rossi MG,  Elevated cerebral blood volume contributes to increased FLAIR signal in the cerebral sulci of propofol-sedated children. AJNR Am J Neuroradiol. 2014;35(8):1574\u20131579."},{"issue":"8","key":"b21","series-title":"AJNR Am J Neuroradiol","first-page":"1487","article-title":"Quantitative cerebrovascular reserve measured by acetazolamide-challenged dynamic CT perfusion in ischemic adult moyamoya disease: initial experience with angiographic correlation","volume":"29","author":"Kang KH","year":"2008","unstructured":"Kang KH, Kim HS, Kim SY. Quantitative cerebrovascular reserve measured by acetazolamide-challenged dynamic CT perfusion in ischemic adult moyamoya disease: initial experience with angiographic correlation. AJNR Am J Neuroradiol. 2008;29(8):1487\u20131493."},{"issue":"5","key":"b22","series-title":"Neurosurgery","first-page":"1009","article-title":"Diffuse leptomeningeal enhancement, \"ivy sign,\" in magnetic resonance images of moyamoya disease in childhood: case report","volume":"37","author":"Ohta T","year":"1995","unstructured":"Ohta T, Tanaka H, Kuroiwa T. Diffuse leptomeningeal enhancement, \"ivy sign,\" in magnetic resonance images of moyamoya disease in childhood: case report. Neurosurgery. 1995;37(5):1009\u20131012."}],"container-title":["Journal of Neurosurgery: Pediatrics"],"original-title":[],"link":[{"URL":"https:\/\/thejns.org\/view\/journals\/j-neurosurg-pediatr\/34\/1\/article-p111.xml","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/thejns.org\/downloadpdf\/journals\/j-neurosurg-pediatr\/34\/1\/article-p111.xml","content-type":"text\/html","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/thejns.org\/downloadpdf\/journals\/j-neurosurg-pediatr\/34\/1\/article-p111.xml","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,12,6]],"date-time":"2024-12-06T13:07:32Z","timestamp":1733490452000},"score":1,"resource":{"primary":{"URL":"https:\/\/thejns.org\/view\/journals\/j-neurosurg-pediatr\/34\/1\/article-p111.xml"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,7,1]]},"references-count":22,"journal-issue":{"issue":"1"},"URL":"https:\/\/doi.org\/10.3171\/2024.2.peds23414","relation":{},"ISSN":["1933-0707","1933-0715"],"issn-type":[{"value":"1933-0707","type":"print"},{"value":"1933-0715","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,7,1]]}}}